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MBE Advance Access published online on June 6, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl034
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted June 1, 2006

Research Article

Evolutionary Origin and Maintenance of Coexpressed Gene Clusters in Mammals

Marie Sémon 1 * and Laurent Duret 2

1 Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558 Université Claude Bernard Lyon 1, 16 rue Raphaël Dubois, 69622 Villeurbanne Cedex, France; Current address : Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland
2 Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558 Université Claude Bernard Lyon 1, 16 rue Raphaël Dubois, 69622 Villeurbanne Cedex, France

* To whom correspondence should be addressed.
Marie Sémon, E-mail: semonm{at}tcd.ie


  Abstract

Gene order is not random with regard to gene expression in mammals: co-expressed genes, and in particular housekeeping genes, are clustered along chromosomes more often than expected by chance. To understand the origin of these clusters, and to quantify the impact of this phenomenon on genome organisation, we analysed clusters of coexpressed genes in the human and mouse genomes. We show that neighboring genes experience continuous concerted expression changes during evolution, which leads to the formation of co-expressed gene clusters. The pattern of expression within these clusters evolves more slowly than the genomic average. Moreover, by studying gene order evolution we show that some clusters are maintained by natural selection, and therefore have a functional significance. However we also demonstrate that some co-expressed gene clusters are the result of neutral coevolution effects, as illustrated by the clustering of genes escaping inactivation on the X chromosome. Moreover, we show that although statistically significant, constraints on gene orders have a limited impact on mammalian genome organization, affecting only 3 to 5% of the pool of human and murine genes. It had been hypothesised that co-expressed genes clusters might correspond to large chromatin domains. In contradiction, we find that most of these clusters contain only two genes whose coexpression may be due to transcriptional read-through or to the activity of bidirectional promoters.

Keywords: cluster; coexpressed genes; chromatin; gene order.
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